Otolaryngology http://oto.sagepub.com/ -- Head and Neck Surgery
Exclusive Endoscopic Resection of Juvenile Nasopharyngeal Angiofibroma: A Systematic Review of the Literature Nadim Khoueir, Nicolas Nicolas, Ziad Rohayem, Amine Haddad and Walid Abou Hamad Otolaryngology -- Head and Neck Surgery 2014 150: 350 originally published online 31 December 2013 DOI: 10.1177/0194599813516605 The online version of this article can be found at: http://oto.sagepub.com/content/150/3/350
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Systematic Review
Exclusive Endoscopic Resection of Juvenile Nasopharyngeal Angiofibroma: A Systematic Review of the Literature
Otolaryngology– Head and Neck Surgery 2014, Vol. 150(3) 350–358 Ó American Academy of Otolaryngology—Head and Neck Surgery Foundation 2013 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/0194599813516605 http://otojournal.org
Nadim Khoueir, MD1, Nicolas Nicolas, MD1, Ziad Rohayem, MD2, Amine Haddad, MD, FRCS1, and Walid Abou Hamad, MD1
No sponsorships or competing interests have been disclosed for this article.
Abstract Objective. To systematically review the exclusive endoscopic treatment of juvenile nasopharyngeal angiofibroma in the literature to define the clinical features in terms of staging and the treatment outcomes in terms of bleeding, recurrence, residual tumor, and complications. Data Sources. Online databases, including PubMed and EMBASE, were used. Reference sections of identified studies were examined for additional articles. Review Methods. The literature was searched by 2 reviewers with the following inclusion criteria: English or French language and exclusive endoscopic treatment of juvenile nasopharyngeal angiofibroma. We were only able to perform a meta-analysis on the categorical outcomes using DerSimonian and Laird random effects models. Results. Ninety-two studies were included with a majority of retrospective studies (54/92; 58.6%). No randomized controlled trials were found. A total of 821 patients were identified. The Radowski classification was the most commonly used (29/92; 31.15%). The mean operative blood loss was 564.21 mL (minimum, 20 mL; maximum, 1482 mL). It was 414.6 mL (minimum, 20 mL; maximum, 1000 mL) and 774.2 mL (minimum, 228 mL; maximum, 1482 mL), respectively, in the group with and without embolization. No conclusion could be made because it was not stratified by tumor stage and because of the absence of randomized controlled trials. The random effect estimate of recurrence was 10% (95% confidence interval [CI], 8.3-11.7). It was 9.3% (95% CI, 7.211.5) for complications and 7.7% (95% CI, 5.4-10.1) for residual tumor. Conclusion. The endoscopic treatment is an evolving modality. It is considered today the treatment of choice. A new classification system based on the endoscopic approach should be proposed in future studies. Keywords juvenile nasopharyngeal angiofibroma, endoscopy, bleeding, complications, recurrence
Received August 6, 2013; revised November 12, 2013; accepted November 21, 2013.
A
ccounting for less than 0.5% of all head and neck tumors, juvenile nasopharyngeal angiofibroma (JNA) is a rare, extremely vascular benign neoplasm almost exclusive to the nasopharynx of adolescent males. These slow-growing lesions originate around the sphenopalatine foramen and initially expand intranasally and then into the pterygomaxillary space. They eventually erode bone and invade the infratemporal fossa, orbit, and middle cranial fossa. Classically, JNA presents with the triad of unilateral nasal obstruction, epistaxis, and a nasopharyngeal mass.1 Juvenile nasopharyngeal angiofibromas can be cured by complete surgical excision. A number of open surgical approaches have been advocated in the literature, including transfacial, transoral, and combined craniofacial procedures.24 All these open procedures share the need to make oral or facial incisions and the need to remove or divide bone to gain access to the tumor. Advances in endoscopic endonasal surgery coupled with the success of preoperative arterial embolization allowed endoscopic management of selected cases. Success is dependent on the surgeon’s experience, skills, and careful patient selection. Recent improvements in techniques and instrumentation as well as the widespread use of this technique among surgeons have broadened its indications from small nasal tumors to those invading the infratemporal fossa in some centers. Endoscopic resection provides several advantages over more traditional surgical techniques, which include the avoidance of facial incisions and plating of the maxilla and
1 Otolaryngology–Head and Neck Surgery, Hotel Dieu de France University Hospital, Saint Joseph University Medical School, Beirut, Lebanon 2 Otolaryngology–Head and Neck Surgery, Saint-Elizabeth Medical Center, Brighton, Massachusetts, USA
Corresponding Author: Nadim Khoueir, MD, Hotel Dieu de France University Hospital, Boulevard Alfred Naccache, BP 16-6830, Beirut, Lebanon. Email: [email protected]
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the minimization of bone removal.5,6 Endoscopes permit a multiangled and magnified view of the tumor and surrounding structures. Many staging systems have been used to define the extent of the tumor. They have a prognosis value and a surgical approach connotation that have been validated in the era of the open surgical technique. A new staging system adapted to the endoscopic approach should be proposed with the recent advance of this technique. Endoscopic resection is becoming the treatment of choice for JNA. It is surgeon dependent, with a whole new set of heterogeneous outcomes in terms of bleeding, recurrence, operative time, hospital stay, and complications. The literature review reveals a lot of reports and a number of reviews with contradictory conclusions with respect to tumor stage classification, type of approaches, the use of preoperative embolization, and outcomes. There are no randomized controlled trials (RCTs) or systematic reviews in the French and English literature as of the time this review was conducted. We performed a systematic review of all published cases of exclusively endoscopically resected JNA from 1995 to 2012, highlighting their respective outcomes in terms of embolization, surgical time, blood loss, hospital stay, complications, and recurrence rate.
Materials and Methods Inclusion and Exclusion Criteria This study was exempt from institutional ethics committee approval, as it was a systematic review of existing published data. It included all studies that reported results on endoscopic treatment of JNA. Studies based solely on the surgical approach and those that did not differentiate between the two methods in the results were excluded. Only studies published in English or French were included.
Literature Search Strategy An online search in PubMed and EMBASE was started in November 2012 for all available articles published using the following combinations of terms: angiofibroma AND endoscopic. Two evaluators independently selected the studies based on titles, excluding those that were not related to the theme of this review. After selection, the evaluators analyzed the abstracts of the selected articles to identify those that met the inclusion criteria. The included studies were then entirely analyzed.
Data extraction and analysis. Data were extracted by 1 reviewer and checked by a second reviewer. We extracted the number of endoscopic resections reported, the stage of the JNA with the staging system, the possibility of previous surgery or embolization, the surgical time, the estimated blood loss, the hospital stay duration, and outcomes on residual tumor and recurrence. Since most studies did not report standard deviation measures for their continuous variables, we were only able to perform a meta-analysis on the categorical outcomes: complications, recurrence, and residual tumor.
We used DerSimonian and Laird random effects models and calculated the estimate of heterogeneity based on the inverse-variance fixed effects model. Confidence intervals (95%) for each proportion were calculated. Analysis was performed using Stata/IC 11.2 (StataCorp LP, College Station, Texas).
Results Literature Search Results The EMBASE search yielded 249 references, and the PubMed search yielded 172 references. The searches were combined. On the basis of the review of titles, 186 articles were excluded because they were either duplicates or did not meet a priori inclusion criteria. In total, 235 abstracts were reviewed, and 71 were excluded because of language or because the studies did not include a purely endoscopic approach. Of the 164 full-text articles assessed for eligibility, 72 were excluded because the outcomes of the purely endoscopic treatment were merged with those of the external or combined approach. In total, 92 studies reporting results on the exclusive endoscopic treatment of JNA were included (Figure 1). All the studies were descriptive. No RCT or comparative studies were available in the literature. Most studies were retrospective (54/92; 58.6%). The remaining were case reports (22/92; 23.9%), case series (9/92; 10%), and prospective (7/ 92; 7.6%) (Table 1). The main features of the studies are summarized in the appendix (available at otojournal.org).
Clinical Data and Outcomes Patient characteristics. A total of 821 patients were identified with an average of 8.9 per study. Cloutier et al7 reported the largest series with 48 patients. Most of the patients are included in retrospective studies (626/821; 76.2%). The history of previous surgery was not reported in 77.7% of cases (683/821). Eighty-one patients (9.68%) had a previous surgery, while 57 patients (6.94%) were primarily treated. Staging. The staging system was not specified in 32.6% (30/ 92) of the studies. The remaining studies used different systems: Radowski in 31.15% (29/92), Fisch in 14.13% (13/ 92), Andrews in 11.95% (11/92), Chandler in 4.34% (4/92); Sessions in 3.26% (3/92), and Bremer in 1.08% (1/92). Multiple staging systems were used in 1 study (Table 2). Embolization and blood loss. Among the 821 patients selected, 564 (68.7%) had an embolization prior to endoscopic resection, while 176 (21.5%) were not embolized. For 81 patients (9.9%), it was not specified whether an embolization was performed. The operative blood loss was reported in a total of 474 cases with a mean of 564.21 mL (minimum, 20 mL7; maximum, 1482 mL8). In the embolization group, the data were available for 252 patients with a mean blood loss of 414.6 mL (minimum, 20 mL7; maximum, 1000 mL9). In the nonembolization group, the data were available for 126 patients
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Idenficaon
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Records idenfied through database searching (n = 421)
Screening
Records excluded based on tle or duplicaon (n = 186)
Eligibility
Records screened (n = 235)
• • •
Included
Full-text arcles assessed for eligibility (n = 164)
Records excluded (n = 71) Language Purely external approach Purely combined approach
Full-text arcles excluded, with reasons (n = 72) • Results merged with external or combined approach • Results merged with other sinonasal tumors
Studies included in qualitave synthesis (n = 92)
Figure 1. Flowchart of study selection.
Table 1. Distribution of study designs among total studies.
Table 2. Distribution of staging systems among total studies.
Study Design
No. of Studies (n = 92)
Percentage
Staging
Retrospective Case reports Case series Prospective
54 22 9 7
58.6 23.9 10.0 7.6
with a mean blood loss of 774.2 mL (minimum, 228 mL10; maximum, 1482 mL8). We were not able to conduct a meta-analysis for numerous reasons. First of all, most of the studies were noncomparative case series that included only 1 surgical technique. Some were even case reports. Moreover, standard deviations were not always reported in the articles, which also hindered the ability to conduct an adequate meta-analysis. And since the blood loss was not stratified by tumor stage in the
Not specified Radowski Fisch Andrews Chandler Sessions Bremer Multiple
No. of Studies (n = 92)
Percentage
30 29 13 11 4 3 1 1
32.6 31.15 14.13 11.95 4.34 3.26 1.08 1.08
majority of studies, no comparison could be done and no definite conclusion could be taken.
Surgical time, hospital stay, and complications. The surgical time was reported in 28 studies, corresponding to 241
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Table 3. Random effect estimate of categorical outcomes. Random Effect Estimate, %
Lower 95% CI
Upper 95% CI
Heterogeneity, Q (P Value)
9.3 7.7 10
7.2 5.4 8.3
11.5 10.1 11.7
3121.136 (\.001) 81.147 (\.001) 115.692 (\.001)
Complications Residual tumor Recurrence Abbreviation: CI, confidence interval.
Table 4. Number of complications following endoscopic treatment of juvenile nasopharyngeal angiofibroma. Complications Not specified No complications Synechia Neurologic disorders Bleeding/buccal hematoma Ocular disorders Facial edema/atrophic rhinitis Eustachian tube dysfunction Cerebrospinal fluid leak
No. of Patients (n = 821) 122 646 19 12 9 5 5 2 1
patients. The mean time was 168.35 minutes with a minimum of 60 minutes11 and a maximum of 321 minutes.12 The duration of hospitalization was reported in 41 studies, corresponding to 454 patients. The mean duration was 4.47 days with a minimum of 1 day13-17 and a maximum of 13 days.18 The complications were reported in 62 studies, corresponding to 699 patients. The random effect estimate of complications was 9.3% (95% confidence interval [CI], 7.211.5). The test for heterogeneity was significant (Q = 3121.136; P \ .001) (Table 3). The complications included synechia (n = 19), neurologic disorders (n = 12), bleeding/ buccal hematoma (n = 9), ocular disorders (n = 5), facial edema or atrophic rhinitis (n = 5), eustachian tube dysfunction (n = 2), and cerebrospinal fluid leak (n = 1) (Table 4).
Residual tumor, follow-up, and recurrences. Residual tumor was mentioned in 15 studies, corresponding to 184 patients. Twelve cases of residual tumor were reported. The random effect estimate of residual tumor was 7.7% (95% CI, 5.410.1). The test for heterogeneity was significant (Q = 81.147; P \ .001) (Table 3). The postoperative follow-up duration was mentioned in 75 studies, corresponding to 701 patients. The mean period could be calculated for only 63 (528 patients) and was 35.6 months (1.5-90 months). Recurrences were mentioned in 81 studies, corresponding to 709 patients. Fifty-eight patients had recurrences during the follow-up period. The random effect estimate of recurrence was 10% (95% CI, 8.3-11.7). The test for heterogeneity was significant (Q = 615.692; P \ .001) (Table 3).
Prospective Studies Patients’ characteristics. In our review, we have found 7 prospective studies8,10,19-23 with 124 patients treated by endoscopic resection of JNA, with an average of 17.7 per study and a maximum of 28.10 We found only 1 prospective comparative study8 that was not a RCT. The others were prospective cohort studies. Eight patients underwent a revision surgery (6.45%), while primary surgery was performed in 55 patients (44.35%). The history of previous surgery was not reported in 61 cases (49.1%). Staging. The most used staging system was Radowski, with 4 studies and 85 patients (68.54%); other staging systems were Bremer (1 study, 12 patients), Chandler (1 study, 8 patients), and Fisch (1 study, 19 patients). Embolization and blood loss. Embolization of the tumor was performed in 86 patients (69.3%) prior to endoscopic surgery, while the rest (38 tumors, 31.7%) were resected without preoperative embolization. Blood loss was reported in 85 patients, with a mean of 605.23 mL, a minimum of 228 mL,10 and a maximum of 1482 mL.10 In the embolization group, mean blood loss was 203.9 mL vs 247.21 mL in nonembolized patients. Surgical time, hospital stay, and complications. The surgical time was reported in 3 studies,8,19,20 corresponding to 50 patients; the mean time was 321.26 minutes (minimum, 10220; maximum, 2698). Hospital stay was reported in 4 studies and 62 patients with a mean of 5.2 days and a range between 2 and 8 days. Complications were reported for 77 patients in 5 studies.10,19,20,22,23 While 73 patients experienced no complications, 1 experienced bleeding, 1 had a neurologic complication, and 1 had a CSF leak. Residual tumor, follow-up, and recurrences. Two studies10,20 with 36 patients mentioned 1 residual tumor after surgery. The follow-up period was mentioned in all 7 prospective studies, but the mean period could be calculated for only 5 (77 patients) and was 18.5 months (12-34 months). Recurrence was observed in 8 patients.
Discussion Although JNA is the most common benign tumor of the nasopharynx, it is an extremely rare pathology with a reported incidence of 0.4 cases per million inhabitants per
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year. It is slightly increased to 3.7 cases per million when considering the population at risk (male adolescents).24 This low incidence makes it difficult to conduct prospective double-blind RCTs and explains the presence of mainly retrospective studies and case series in the literature. A shift in the surgical paradigm of JNA has been observed with the introduction of the endoscopic technique as an alternative to the classic external surgical approach. The endoscopic technique has evolved during the past 2 decades, pushing gradually the boundaries of its indications. This evolution is not based on evidence but on the results of some series published gradually in the literature. Although a meta-analysis based on high-level comparative studies is impossible, a systematic review of the literature is needed to analyze all what has been published on the endoscopic treatment of JNA. Recently, Boghani et al25 published a systematic review aiming to compare the endoscopic, endoscopic-assisted, and external surgical treatment. They reviewed studies that reported simultaneously all the outcomes defined in the objectives and reported a total of 308 cases treated by the exclusive endoscopic technique. Knowing that no true comparison can be made with the available literature, we wanted to analyze all the exclusive endoscopic approach cases if the study reported any of the predefined outcomes. We also reported alone the prospective studies that represent the highest level of evidence available. This explains why we had 821 cases in our review that did not include the endoscopic-assisted and the external surgical approaches.
Staging Systems A good staging system should be universal, have a prognostic value, and have a therapeutic correlation. Many staging systems have been proposed and used variably in the literature. We found that Radowski26 was the most commonly reported (31.15%), followed by Fisch27 (14.13%), Andrews28 (11.95%), Chandler29 (4.34%), Sessions30 (3.26%), and Bremer26 (1.08%). These staging systems were established in the 1980s or early 1990s, when the external surgical approach was the only treatment modality available. A new staging system is thus needed and should be adapted to the boundaries and limitations of the endoscopic technique. These boundaries are still poorly defined but gradually pushed toward more advanced tumors. This staging system would thus guide the endoscopic treatment, define its limits, provide a prognostic value, and be universally adapted in the future series. Future studies should homogeneously mention these boundaries knowing that 32.6% of the previous studies did not specify any extension information.
Surgical Technique In the past, the external surgical approach was the only method used for JNA resection. A transpalatal approach was warranted for tumors confined to the nasopharynx. A gingivobuccal incision was added to gain access to the pterygomaxillary area. A lateral rhinotomy with resection of the medial antral wall was warranted for tumors that involved
the nasal fossa and/or the pterygopalatine fossa. A transnasal/transantral approach was used for tumors extended to the infratemporal fossa.31 The first report of endoscopic surgery for JNA was published in 1996 by Kamel.32 It was proposed for tumors limited to the nasopharynx, nasal cavity, ethmoid sinuses, and sphenoid sinuses. Significant involvement of the pterygopalatine or infratemporal fossae has been regarded by most surgeons as a contraindication to a purely endoscopic approach. Carrau et al13 treated successfully these advanced tumors by endoscopy alone. Many advantages have been attributed to this technique7: better exposure, allowing a good visualization of lateral or very deep areas, such as the clivus, foramen lacerum, roots of pterygoid, or infratemporal fossa. Furthermore, avoiding external incisions, soft tissue detachment, and anterior skeletal osteotomies is probably associated with a reduced pre- and postoperative morbidity. Cloutier et al7 published recently the largest series in a retrospective review of 48 cases. During the period extending from April 2000 to June 2005 (group 1), patients eligible for an endoscopic approach had a tumor limited to the sinuses, pterygopalatine fossa, medial infratemporal fossa, or root of the pterygoids, with a limited volume. Massive and large tumors were treated through an external approach. However, during the period extending from July 2005 to August 2010 (group 2), all tumors were treated by endoscopy alone except in cases of massive middle fossa invasion, optic nerve, or internal carotid artery encasement. No statistical difference was found between the 2 groups concerning the rate of recurrence and complications. Moreover, 29 cases classified as Radowski stage IIIA (minimal intracranial extension) were successfully treated by endoscopy alone. The intracranial boundary was pushed further by Mohammadi et al,8 who treated 5 cases endoscopically with Radowski stage IIIB (extensive intracranial extension). We found in our review 54 cases (6.4%) of intracranial JNA treated by endoscopy alone.
Complications and Blood Loss A complication rate of 9.3% (random effect estimate; 95% CI, 7.2-11.5) was found with the endoscopic technique, the most common being synechia, followed by neurologic disorder (mainly infraorbital nerve hypoesthesia), bleeding/ buccal hematoma, ocular disorders, facial edema, atrophic rhinitis, eustachian tube dysfunction, and 1 case of cerebrospinal fluid leak. Blood loss is a major factor that should be reported. The data were missing for 42.2% of patients. The mean value was 564.21 mL. We found an increase in blood loss in the nonembolization group (774.2 mL) compared with the embolization group (414.6 mL). However, we could not draw any conclusion since the blood loss was not stratified by tumor stage and since there were no RCTs in the literature. We found a small difference when the data were taken from prospective studies only with a mean blood loss of 247.21 mL in the nonembolization group and 203.9 mL in the embolization group. The difference could be due to the limited number of cases reported in the prospective studies. Ardehali et al33 published the largest series of JNA
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treated endoscopically without embolization. The 42 cases had a mean blood loss of 1403 mL, with 32 patients requiring transfusion. Only 5 cases had a preoperative embolization. Their mean blood loss was 770 mL, and no transfusion was needed in this group. However Mohammadi et al8 showed no difference in mean blood loss between the 2 groups in a prospective study including 8 cases of intracranial tumors with no difference in staging between the 2 groups. Thus, embolization is widely used prior to endoscopic resection of JNA with a hypothetical effect in reducing intraoperative blood loss. Comparative studies would be difficult to conduct, mainly for ethical reasons.
Residual Tumors The presence of residual tumors was only mentioned in 15 studies reporting 12 positive cases. The random effect estimate was 7.7% (95% CI, 5.4-10.1). It is an important factor that should be reported in future studies because it is an indirect marker of the limits of the endoscopic resection. Moreover, the patient’s age should be mentioned since it is intimately related to growth rate and, in consequence, to the residual tumor’s natural history.
tumors. It is an accepted and widely used technique even in the absence of studies with a high level of evidence. Future studies should report some important information such as staging, embolization, bleeding, follow-up, recurrence, residual tumor, and age of resection. A new staging based on the endoscopic boundaries should also be proposed. Acknowledgment Dany Matar, MD, MPH, provided statistical analysis.
Author Contributions Nadim Khoueir, conception, data analysis, drafting, final approval; Nicolas Nicolas, conception, data analysis, drafting, final approval; Ziad Rohayem, conception, data analysis, drafting, final approval; Amine Haddad, supervision, conception, data analysis, drafting, final approval; Walid Abou Hamad, study design, supervision, conception, data analysis, drafting, final approval.
Disclosures Competing interests: None. Sponsorships: None. Funding source: None.
Recurrence
Supplemental Material
The recurrence was mentioned in the majority of the studies (81/92) with variable follow-up periods. A small number of recurrences (n = 58) were reported. The recurrence rate of 10% (random effect estimate; 95% CI, 8.3-11.7) is lower than the values reported for the external surgical approach (14.5%).25 Thus, the endoscopic technique is at least as good as the external technique regarding the recurrence rate. Again, no recommendations can be done in the absence of studies of a high level of evidence comparing the 2 techniques. Such studies are also difficult to conduct for the same reasons mentioned above.
Additional supporting information may be found at http://oto.sage pub.com/content/by/supplemental-data
Limitations Some limitations in this study should be noted. First of all, we did not review the combined and the external surgical treatments of JNA. We considered that in the absence of RCT, any comparison of results would not lead to certified conclusions and recommendations based on evidence. However, it could give us some comparative information. Moreover, we reviewed all the studies7-24,31-104 that reported on the endoscopic treatment of JNA, including case reports and studies lacking some information such as follow-up, recurrence, or staging. We considered that in the absence of a comparative intension, a descriptive systematic review should include all the cases reported in the literature. Moreover, by reporting the weaknesses encountered, we can propose some recommendations for the future studies.
Conclusion In conclusion, the endoscopic treatment is an evolving treatment modality of JNA, and its limits are progressively pushed further. The results are promising in terms of morbidity and tumor control even for advanced and intracranial
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Exclusive Endoscopic Resection of Juvenile Nasopharyngeal Angiofibroma: A Systematic Review of the Literature Nadim Khoueir, Nicolas Nicolas, Ziad Rohayem, Amine Haddad and Walid Abou Hamad Otolaryngology -- Head and Neck Surgery 2014 150: 350 originally published online 31 December 2013 DOI: 10.1177/0194599813516605 The online version of this article can be found at: http://oto.sagepub.com/content/150/3/350
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Systematic Review
Exclusive Endoscopic Resection of Juvenile Nasopharyngeal Angiofibroma: A Systematic Review of the Literature
Otolaryngology– Head and Neck Surgery 2014, Vol. 150(3) 350–358 Ó American Academy of Otolaryngology—Head and Neck Surgery Foundation 2013 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/0194599813516605 http://otojournal.org
Nadim Khoueir, MD1, Nicolas Nicolas, MD1, Ziad Rohayem, MD2, Amine Haddad, MD, FRCS1, and Walid Abou Hamad, MD1
No sponsorships or competing interests have been disclosed for this article.
Abstract Objective. To systematically review the exclusive endoscopic treatment of juvenile nasopharyngeal angiofibroma in the literature to define the clinical features in terms of staging and the treatment outcomes in terms of bleeding, recurrence, residual tumor, and complications. Data Sources. Online databases, including PubMed and EMBASE, were used. Reference sections of identified studies were examined for additional articles. Review Methods. The literature was searched by 2 reviewers with the following inclusion criteria: English or French language and exclusive endoscopic treatment of juvenile nasopharyngeal angiofibroma. We were only able to perform a meta-analysis on the categorical outcomes using DerSimonian and Laird random effects models. Results. Ninety-two studies were included with a majority of retrospective studies (54/92; 58.6%). No randomized controlled trials were found. A total of 821 patients were identified. The Radowski classification was the most commonly used (29/92; 31.15%). The mean operative blood loss was 564.21 mL (minimum, 20 mL; maximum, 1482 mL). It was 414.6 mL (minimum, 20 mL; maximum, 1000 mL) and 774.2 mL (minimum, 228 mL; maximum, 1482 mL), respectively, in the group with and without embolization. No conclusion could be made because it was not stratified by tumor stage and because of the absence of randomized controlled trials. The random effect estimate of recurrence was 10% (95% confidence interval [CI], 8.3-11.7). It was 9.3% (95% CI, 7.211.5) for complications and 7.7% (95% CI, 5.4-10.1) for residual tumor. Conclusion. The endoscopic treatment is an evolving modality. It is considered today the treatment of choice. A new classification system based on the endoscopic approach should be proposed in future studies. Keywords juvenile nasopharyngeal angiofibroma, endoscopy, bleeding, complications, recurrence
Received August 6, 2013; revised November 12, 2013; accepted November 21, 2013.
A
ccounting for less than 0.5% of all head and neck tumors, juvenile nasopharyngeal angiofibroma (JNA) is a rare, extremely vascular benign neoplasm almost exclusive to the nasopharynx of adolescent males. These slow-growing lesions originate around the sphenopalatine foramen and initially expand intranasally and then into the pterygomaxillary space. They eventually erode bone and invade the infratemporal fossa, orbit, and middle cranial fossa. Classically, JNA presents with the triad of unilateral nasal obstruction, epistaxis, and a nasopharyngeal mass.1 Juvenile nasopharyngeal angiofibromas can be cured by complete surgical excision. A number of open surgical approaches have been advocated in the literature, including transfacial, transoral, and combined craniofacial procedures.24 All these open procedures share the need to make oral or facial incisions and the need to remove or divide bone to gain access to the tumor. Advances in endoscopic endonasal surgery coupled with the success of preoperative arterial embolization allowed endoscopic management of selected cases. Success is dependent on the surgeon’s experience, skills, and careful patient selection. Recent improvements in techniques and instrumentation as well as the widespread use of this technique among surgeons have broadened its indications from small nasal tumors to those invading the infratemporal fossa in some centers. Endoscopic resection provides several advantages over more traditional surgical techniques, which include the avoidance of facial incisions and plating of the maxilla and
1 Otolaryngology–Head and Neck Surgery, Hotel Dieu de France University Hospital, Saint Joseph University Medical School, Beirut, Lebanon 2 Otolaryngology–Head and Neck Surgery, Saint-Elizabeth Medical Center, Brighton, Massachusetts, USA
Corresponding Author: Nadim Khoueir, MD, Hotel Dieu de France University Hospital, Boulevard Alfred Naccache, BP 16-6830, Beirut, Lebanon. Email: [email protected]
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the minimization of bone removal.5,6 Endoscopes permit a multiangled and magnified view of the tumor and surrounding structures. Many staging systems have been used to define the extent of the tumor. They have a prognosis value and a surgical approach connotation that have been validated in the era of the open surgical technique. A new staging system adapted to the endoscopic approach should be proposed with the recent advance of this technique. Endoscopic resection is becoming the treatment of choice for JNA. It is surgeon dependent, with a whole new set of heterogeneous outcomes in terms of bleeding, recurrence, operative time, hospital stay, and complications. The literature review reveals a lot of reports and a number of reviews with contradictory conclusions with respect to tumor stage classification, type of approaches, the use of preoperative embolization, and outcomes. There are no randomized controlled trials (RCTs) or systematic reviews in the French and English literature as of the time this review was conducted. We performed a systematic review of all published cases of exclusively endoscopically resected JNA from 1995 to 2012, highlighting their respective outcomes in terms of embolization, surgical time, blood loss, hospital stay, complications, and recurrence rate.
Materials and Methods Inclusion and Exclusion Criteria This study was exempt from institutional ethics committee approval, as it was a systematic review of existing published data. It included all studies that reported results on endoscopic treatment of JNA. Studies based solely on the surgical approach and those that did not differentiate between the two methods in the results were excluded. Only studies published in English or French were included.
Literature Search Strategy An online search in PubMed and EMBASE was started in November 2012 for all available articles published using the following combinations of terms: angiofibroma AND endoscopic. Two evaluators independently selected the studies based on titles, excluding those that were not related to the theme of this review. After selection, the evaluators analyzed the abstracts of the selected articles to identify those that met the inclusion criteria. The included studies were then entirely analyzed.
Data extraction and analysis. Data were extracted by 1 reviewer and checked by a second reviewer. We extracted the number of endoscopic resections reported, the stage of the JNA with the staging system, the possibility of previous surgery or embolization, the surgical time, the estimated blood loss, the hospital stay duration, and outcomes on residual tumor and recurrence. Since most studies did not report standard deviation measures for their continuous variables, we were only able to perform a meta-analysis on the categorical outcomes: complications, recurrence, and residual tumor.
We used DerSimonian and Laird random effects models and calculated the estimate of heterogeneity based on the inverse-variance fixed effects model. Confidence intervals (95%) for each proportion were calculated. Analysis was performed using Stata/IC 11.2 (StataCorp LP, College Station, Texas).
Results Literature Search Results The EMBASE search yielded 249 references, and the PubMed search yielded 172 references. The searches were combined. On the basis of the review of titles, 186 articles were excluded because they were either duplicates or did not meet a priori inclusion criteria. In total, 235 abstracts were reviewed, and 71 were excluded because of language or because the studies did not include a purely endoscopic approach. Of the 164 full-text articles assessed for eligibility, 72 were excluded because the outcomes of the purely endoscopic treatment were merged with those of the external or combined approach. In total, 92 studies reporting results on the exclusive endoscopic treatment of JNA were included (Figure 1). All the studies were descriptive. No RCT or comparative studies were available in the literature. Most studies were retrospective (54/92; 58.6%). The remaining were case reports (22/92; 23.9%), case series (9/92; 10%), and prospective (7/ 92; 7.6%) (Table 1). The main features of the studies are summarized in the appendix (available at otojournal.org).
Clinical Data and Outcomes Patient characteristics. A total of 821 patients were identified with an average of 8.9 per study. Cloutier et al7 reported the largest series with 48 patients. Most of the patients are included in retrospective studies (626/821; 76.2%). The history of previous surgery was not reported in 77.7% of cases (683/821). Eighty-one patients (9.68%) had a previous surgery, while 57 patients (6.94%) were primarily treated. Staging. The staging system was not specified in 32.6% (30/ 92) of the studies. The remaining studies used different systems: Radowski in 31.15% (29/92), Fisch in 14.13% (13/ 92), Andrews in 11.95% (11/92), Chandler in 4.34% (4/92); Sessions in 3.26% (3/92), and Bremer in 1.08% (1/92). Multiple staging systems were used in 1 study (Table 2). Embolization and blood loss. Among the 821 patients selected, 564 (68.7%) had an embolization prior to endoscopic resection, while 176 (21.5%) were not embolized. For 81 patients (9.9%), it was not specified whether an embolization was performed. The operative blood loss was reported in a total of 474 cases with a mean of 564.21 mL (minimum, 20 mL7; maximum, 1482 mL8). In the embolization group, the data were available for 252 patients with a mean blood loss of 414.6 mL (minimum, 20 mL7; maximum, 1000 mL9). In the nonembolization group, the data were available for 126 patients
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Idenficaon
352
Records idenfied through database searching (n = 421)
Screening
Records excluded based on tle or duplicaon (n = 186)
Eligibility
Records screened (n = 235)
• • •
Included
Full-text arcles assessed for eligibility (n = 164)
Records excluded (n = 71) Language Purely external approach Purely combined approach
Full-text arcles excluded, with reasons (n = 72) • Results merged with external or combined approach • Results merged with other sinonasal tumors
Studies included in qualitave synthesis (n = 92)
Figure 1. Flowchart of study selection.
Table 1. Distribution of study designs among total studies.
Table 2. Distribution of staging systems among total studies.
Study Design
No. of Studies (n = 92)
Percentage
Staging
Retrospective Case reports Case series Prospective
54 22 9 7
58.6 23.9 10.0 7.6
with a mean blood loss of 774.2 mL (minimum, 228 mL10; maximum, 1482 mL8). We were not able to conduct a meta-analysis for numerous reasons. First of all, most of the studies were noncomparative case series that included only 1 surgical technique. Some were even case reports. Moreover, standard deviations were not always reported in the articles, which also hindered the ability to conduct an adequate meta-analysis. And since the blood loss was not stratified by tumor stage in the
Not specified Radowski Fisch Andrews Chandler Sessions Bremer Multiple
No. of Studies (n = 92)
Percentage
30 29 13 11 4 3 1 1
32.6 31.15 14.13 11.95 4.34 3.26 1.08 1.08
majority of studies, no comparison could be done and no definite conclusion could be taken.
Surgical time, hospital stay, and complications. The surgical time was reported in 28 studies, corresponding to 241
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Table 3. Random effect estimate of categorical outcomes. Random Effect Estimate, %
Lower 95% CI
Upper 95% CI
Heterogeneity, Q (P Value)
9.3 7.7 10
7.2 5.4 8.3
11.5 10.1 11.7
3121.136 (\.001) 81.147 (\.001) 115.692 (\.001)
Complications Residual tumor Recurrence Abbreviation: CI, confidence interval.
Table 4. Number of complications following endoscopic treatment of juvenile nasopharyngeal angiofibroma. Complications Not specified No complications Synechia Neurologic disorders Bleeding/buccal hematoma Ocular disorders Facial edema/atrophic rhinitis Eustachian tube dysfunction Cerebrospinal fluid leak
No. of Patients (n = 821) 122 646 19 12 9 5 5 2 1
patients. The mean time was 168.35 minutes with a minimum of 60 minutes11 and a maximum of 321 minutes.12 The duration of hospitalization was reported in 41 studies, corresponding to 454 patients. The mean duration was 4.47 days with a minimum of 1 day13-17 and a maximum of 13 days.18 The complications were reported in 62 studies, corresponding to 699 patients. The random effect estimate of complications was 9.3% (95% confidence interval [CI], 7.211.5). The test for heterogeneity was significant (Q = 3121.136; P \ .001) (Table 3). The complications included synechia (n = 19), neurologic disorders (n = 12), bleeding/ buccal hematoma (n = 9), ocular disorders (n = 5), facial edema or atrophic rhinitis (n = 5), eustachian tube dysfunction (n = 2), and cerebrospinal fluid leak (n = 1) (Table 4).
Residual tumor, follow-up, and recurrences. Residual tumor was mentioned in 15 studies, corresponding to 184 patients. Twelve cases of residual tumor were reported. The random effect estimate of residual tumor was 7.7% (95% CI, 5.410.1). The test for heterogeneity was significant (Q = 81.147; P \ .001) (Table 3). The postoperative follow-up duration was mentioned in 75 studies, corresponding to 701 patients. The mean period could be calculated for only 63 (528 patients) and was 35.6 months (1.5-90 months). Recurrences were mentioned in 81 studies, corresponding to 709 patients. Fifty-eight patients had recurrences during the follow-up period. The random effect estimate of recurrence was 10% (95% CI, 8.3-11.7). The test for heterogeneity was significant (Q = 615.692; P \ .001) (Table 3).
Prospective Studies Patients’ characteristics. In our review, we have found 7 prospective studies8,10,19-23 with 124 patients treated by endoscopic resection of JNA, with an average of 17.7 per study and a maximum of 28.10 We found only 1 prospective comparative study8 that was not a RCT. The others were prospective cohort studies. Eight patients underwent a revision surgery (6.45%), while primary surgery was performed in 55 patients (44.35%). The history of previous surgery was not reported in 61 cases (49.1%). Staging. The most used staging system was Radowski, with 4 studies and 85 patients (68.54%); other staging systems were Bremer (1 study, 12 patients), Chandler (1 study, 8 patients), and Fisch (1 study, 19 patients). Embolization and blood loss. Embolization of the tumor was performed in 86 patients (69.3%) prior to endoscopic surgery, while the rest (38 tumors, 31.7%) were resected without preoperative embolization. Blood loss was reported in 85 patients, with a mean of 605.23 mL, a minimum of 228 mL,10 and a maximum of 1482 mL.10 In the embolization group, mean blood loss was 203.9 mL vs 247.21 mL in nonembolized patients. Surgical time, hospital stay, and complications. The surgical time was reported in 3 studies,8,19,20 corresponding to 50 patients; the mean time was 321.26 minutes (minimum, 10220; maximum, 2698). Hospital stay was reported in 4 studies and 62 patients with a mean of 5.2 days and a range between 2 and 8 days. Complications were reported for 77 patients in 5 studies.10,19,20,22,23 While 73 patients experienced no complications, 1 experienced bleeding, 1 had a neurologic complication, and 1 had a CSF leak. Residual tumor, follow-up, and recurrences. Two studies10,20 with 36 patients mentioned 1 residual tumor after surgery. The follow-up period was mentioned in all 7 prospective studies, but the mean period could be calculated for only 5 (77 patients) and was 18.5 months (12-34 months). Recurrence was observed in 8 patients.
Discussion Although JNA is the most common benign tumor of the nasopharynx, it is an extremely rare pathology with a reported incidence of 0.4 cases per million inhabitants per
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year. It is slightly increased to 3.7 cases per million when considering the population at risk (male adolescents).24 This low incidence makes it difficult to conduct prospective double-blind RCTs and explains the presence of mainly retrospective studies and case series in the literature. A shift in the surgical paradigm of JNA has been observed with the introduction of the endoscopic technique as an alternative to the classic external surgical approach. The endoscopic technique has evolved during the past 2 decades, pushing gradually the boundaries of its indications. This evolution is not based on evidence but on the results of some series published gradually in the literature. Although a meta-analysis based on high-level comparative studies is impossible, a systematic review of the literature is needed to analyze all what has been published on the endoscopic treatment of JNA. Recently, Boghani et al25 published a systematic review aiming to compare the endoscopic, endoscopic-assisted, and external surgical treatment. They reviewed studies that reported simultaneously all the outcomes defined in the objectives and reported a total of 308 cases treated by the exclusive endoscopic technique. Knowing that no true comparison can be made with the available literature, we wanted to analyze all the exclusive endoscopic approach cases if the study reported any of the predefined outcomes. We also reported alone the prospective studies that represent the highest level of evidence available. This explains why we had 821 cases in our review that did not include the endoscopic-assisted and the external surgical approaches.
Staging Systems A good staging system should be universal, have a prognostic value, and have a therapeutic correlation. Many staging systems have been proposed and used variably in the literature. We found that Radowski26 was the most commonly reported (31.15%), followed by Fisch27 (14.13%), Andrews28 (11.95%), Chandler29 (4.34%), Sessions30 (3.26%), and Bremer26 (1.08%). These staging systems were established in the 1980s or early 1990s, when the external surgical approach was the only treatment modality available. A new staging system is thus needed and should be adapted to the boundaries and limitations of the endoscopic technique. These boundaries are still poorly defined but gradually pushed toward more advanced tumors. This staging system would thus guide the endoscopic treatment, define its limits, provide a prognostic value, and be universally adapted in the future series. Future studies should homogeneously mention these boundaries knowing that 32.6% of the previous studies did not specify any extension information.
Surgical Technique In the past, the external surgical approach was the only method used for JNA resection. A transpalatal approach was warranted for tumors confined to the nasopharynx. A gingivobuccal incision was added to gain access to the pterygomaxillary area. A lateral rhinotomy with resection of the medial antral wall was warranted for tumors that involved
the nasal fossa and/or the pterygopalatine fossa. A transnasal/transantral approach was used for tumors extended to the infratemporal fossa.31 The first report of endoscopic surgery for JNA was published in 1996 by Kamel.32 It was proposed for tumors limited to the nasopharynx, nasal cavity, ethmoid sinuses, and sphenoid sinuses. Significant involvement of the pterygopalatine or infratemporal fossae has been regarded by most surgeons as a contraindication to a purely endoscopic approach. Carrau et al13 treated successfully these advanced tumors by endoscopy alone. Many advantages have been attributed to this technique7: better exposure, allowing a good visualization of lateral or very deep areas, such as the clivus, foramen lacerum, roots of pterygoid, or infratemporal fossa. Furthermore, avoiding external incisions, soft tissue detachment, and anterior skeletal osteotomies is probably associated with a reduced pre- and postoperative morbidity. Cloutier et al7 published recently the largest series in a retrospective review of 48 cases. During the period extending from April 2000 to June 2005 (group 1), patients eligible for an endoscopic approach had a tumor limited to the sinuses, pterygopalatine fossa, medial infratemporal fossa, or root of the pterygoids, with a limited volume. Massive and large tumors were treated through an external approach. However, during the period extending from July 2005 to August 2010 (group 2), all tumors were treated by endoscopy alone except in cases of massive middle fossa invasion, optic nerve, or internal carotid artery encasement. No statistical difference was found between the 2 groups concerning the rate of recurrence and complications. Moreover, 29 cases classified as Radowski stage IIIA (minimal intracranial extension) were successfully treated by endoscopy alone. The intracranial boundary was pushed further by Mohammadi et al,8 who treated 5 cases endoscopically with Radowski stage IIIB (extensive intracranial extension). We found in our review 54 cases (6.4%) of intracranial JNA treated by endoscopy alone.
Complications and Blood Loss A complication rate of 9.3% (random effect estimate; 95% CI, 7.2-11.5) was found with the endoscopic technique, the most common being synechia, followed by neurologic disorder (mainly infraorbital nerve hypoesthesia), bleeding/ buccal hematoma, ocular disorders, facial edema, atrophic rhinitis, eustachian tube dysfunction, and 1 case of cerebrospinal fluid leak. Blood loss is a major factor that should be reported. The data were missing for 42.2% of patients. The mean value was 564.21 mL. We found an increase in blood loss in the nonembolization group (774.2 mL) compared with the embolization group (414.6 mL). However, we could not draw any conclusion since the blood loss was not stratified by tumor stage and since there were no RCTs in the literature. We found a small difference when the data were taken from prospective studies only with a mean blood loss of 247.21 mL in the nonembolization group and 203.9 mL in the embolization group. The difference could be due to the limited number of cases reported in the prospective studies. Ardehali et al33 published the largest series of JNA
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treated endoscopically without embolization. The 42 cases had a mean blood loss of 1403 mL, with 32 patients requiring transfusion. Only 5 cases had a preoperative embolization. Their mean blood loss was 770 mL, and no transfusion was needed in this group. However Mohammadi et al8 showed no difference in mean blood loss between the 2 groups in a prospective study including 8 cases of intracranial tumors with no difference in staging between the 2 groups. Thus, embolization is widely used prior to endoscopic resection of JNA with a hypothetical effect in reducing intraoperative blood loss. Comparative studies would be difficult to conduct, mainly for ethical reasons.
Residual Tumors The presence of residual tumors was only mentioned in 15 studies reporting 12 positive cases. The random effect estimate was 7.7% (95% CI, 5.4-10.1). It is an important factor that should be reported in future studies because it is an indirect marker of the limits of the endoscopic resection. Moreover, the patient’s age should be mentioned since it is intimately related to growth rate and, in consequence, to the residual tumor’s natural history.
tumors. It is an accepted and widely used technique even in the absence of studies with a high level of evidence. Future studies should report some important information such as staging, embolization, bleeding, follow-up, recurrence, residual tumor, and age of resection. A new staging based on the endoscopic boundaries should also be proposed. Acknowledgment Dany Matar, MD, MPH, provided statistical analysis.
Author Contributions Nadim Khoueir, conception, data analysis, drafting, final approval; Nicolas Nicolas, conception, data analysis, drafting, final approval; Ziad Rohayem, conception, data analysis, drafting, final approval; Amine Haddad, supervision, conception, data analysis, drafting, final approval; Walid Abou Hamad, study design, supervision, conception, data analysis, drafting, final approval.
Disclosures Competing interests: None. Sponsorships: None. Funding source: None.
Recurrence
Supplemental Material
The recurrence was mentioned in the majority of the studies (81/92) with variable follow-up periods. A small number of recurrences (n = 58) were reported. The recurrence rate of 10% (random effect estimate; 95% CI, 8.3-11.7) is lower than the values reported for the external surgical approach (14.5%).25 Thus, the endoscopic technique is at least as good as the external technique regarding the recurrence rate. Again, no recommendations can be done in the absence of studies of a high level of evidence comparing the 2 techniques. Such studies are also difficult to conduct for the same reasons mentioned above.
Additional supporting information may be found at http://oto.sage pub.com/content/by/supplemental-data
Limitations Some limitations in this study should be noted. First of all, we did not review the combined and the external surgical treatments of JNA. We considered that in the absence of RCT, any comparison of results would not lead to certified conclusions and recommendations based on evidence. However, it could give us some comparative information. Moreover, we reviewed all the studies7-24,31-104 that reported on the endoscopic treatment of JNA, including case reports and studies lacking some information such as follow-up, recurrence, or staging. We considered that in the absence of a comparative intension, a descriptive systematic review should include all the cases reported in the literature. Moreover, by reporting the weaknesses encountered, we can propose some recommendations for the future studies.
Conclusion In conclusion, the endoscopic treatment is an evolving treatment modality of JNA, and its limits are progressively pushed further. The results are promising in terms of morbidity and tumor control even for advanced and intracranial
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